Chronic-plus-binge alcohol intake induces production of proinflammatory mtDNA-enriched extracellular vesicles and steatohepatitis via ASK1/p38MAPKα-dependent mechanisms

JCI Insight. 2020 Jul 23;5(14):e136496. doi: 10.1172/jci.insight.136496.

Abstract

Alcohol-associated liver disease is a spectrum of liver disorders with histopathological changes ranging from simple steatosis to steatohepatitis, cirrhosis, and hepatocellular carcinoma. Recent data suggest that chronic-plus-binge ethanol intake induces steatohepatitis by promoting release by hepatocytes of proinflammatory mitochondrial DNA-enriched (mtDNA-enriched) extracellular vesicles (EVs). The aim of the present study was to investigate the role of the stress kinase apoptosis signal-regulating kinase 1 (ASK1) and p38 mitogen-activated protein kinase (p38) in chronic-plus-binge ethanol-induced steatohepatitis and mtDNA-enriched EV release. Microarray analysis revealed the greatest hepatic upregulation of metallothionein 1 and 2 (Mt1/2), which encode 2 of the most potent antioxidant proteins. Genetic deletion of the Mt1 and Mt2 genes aggravated ethanol-induced liver injury, as evidenced by elevation of serum ALT, neutrophil infiltration, oxidative stress, and ASK1/p38 activation in the liver. Inhibition or genetic deletion of Ask1 or p38 ameliorated ethanol-induced liver injury, inflammation, ROS levels, and expression of phagocytic oxidase and ER stress markers in the liver. In addition, inhibition of ASK1 or p38 also attenuated ethanol-induced mtDNA-enriched EV secretion from hepatocytes. Taken together, these findings indicate that induction of hepatic mtDNA-enriched EVs by ethanol is dependent on ASK1 and p38, thereby promoting alcoholic steatohepatitis.

Keywords: Hepatology; Toxicology.

Publication types

  • Research Support, N.I.H., Intramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alcoholism / complications
  • Alcoholism / genetics
  • Alcoholism / pathology
  • Alcohols / toxicity
  • Animals
  • Binge Drinking / complications
  • Binge Drinking / genetics
  • Binge Drinking / pathology
  • DNA, Mitochondrial / genetics
  • Disease Models, Animal
  • Extracellular Vesicles / drug effects
  • Extracellular Vesicles / genetics*
  • Fatty Liver, Alcoholic / etiology
  • Fatty Liver, Alcoholic / genetics*
  • Fatty Liver, Alcoholic / pathology
  • Hepatocytes / drug effects
  • Humans
  • Inflammation / etiology
  • Inflammation / genetics*
  • Inflammation / pathology
  • Liver / drug effects
  • MAP Kinase Kinase Kinase 5 / genetics*
  • Matrix Metalloproteinase 14 / genetics
  • Metallothionein / genetics
  • Mice
  • Signal Transduction / drug effects
  • p38 Mitogen-Activated Protein Kinases / genetics*

Substances

  • Alcohols
  • DNA, Mitochondrial
  • Mt2 protein, mouse
  • Metallothionein
  • p38 Mitogen-Activated Protein Kinases
  • MAP Kinase Kinase Kinase 5
  • Matrix Metalloproteinase 14